Magnetic resonance imaging biomarkers for chronic kidney disease: a position paper from the European Cooperation in Science and Technology Action PARENCHIMA

Abstract Functional renal magnetic resonance imaging (MRI) has seen a number of recent advances, and techniques are now available that can generate quantitative imaging biomarkers with the potential to improve the management of kidney disease. Such biomarkers are sensitive to changes in renal blood flow, tissue perfusion, oxygenation and microstructure (including inflammation and fibrosis), processes that are important in a range of renal diseases including chronic kidney disease. However, several challenges remain to move these techniques towards clinical adoption, from technical validation through biological and clinical validation, to demonstration of cost-effectiveness and regulatory qualification. To address these challenges, the European Cooperation in Science and Technology Action PARENCHIMA was initiated in early 2017. PARENCHIMA is a multidisciplinary pan-European network with an overarching aim of eliminating the main barriers to the broader evaluation, commercial exploitation and clinical use of renal MRI biomarkers. This position paper lays out PARENCHIMA’s vision on key clinical questions that MRI must address to become more widely used in patients with kidney disease, first within research settings and ultimately in clinical practice. We then present a series of practical recommendations to accelerate the study and translation of these techniques.

[1]  W. G. Walker,et al.  Plasma aldosterone regulation in anephric man. , 1973, Kidney international.

[2]  D. Le Bihan,et al.  Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. , 1988, Radiology.

[3]  B. Brenner,et al.  Brenner & Rector's the Kidney , 1996 .

[4]  The Gisen Group.  Randomised placebo-controlled trial of effect of ramipril on decline in glomerular filtration rate and risk of terminal renal failure in proteinuric, non-diabetic nephropathy , 1997, The Lancet.

[5]  Randomised placebo-controlled trial of effect of ramipril on decline in glomerular filtration rate and risk of terminal renal failure in proteinuric, non-diabetic nephropathy. The GISEN Group (Gruppo Italiano di Studi Epidemiologici in Nefrologia) , 1997, Lancet.

[6]  P. F. Kauff.  Group , 2000, Elegant Design.

[7]  P K Commean,et al.  Volumetric Measurement of Renal Cysts and Parenchyma Using MRI: Phantoms and Patients with Polycystic Kidney Disease , 2000, Journal of computer assisted tomography.

[8]  B. Brenner,et al.  Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. , 2001, The New England journal of medicine.

[9]  N. Rofsky,et al.  MR imaging relaxation times of abdominal and pelvic tissues measured in vivo at 3.0 T: preliminary results. , 2004, Radiology.

[10]  F. Dekker,et al.  Screening strategies for chronic kidney disease in the general population: follow-up of cross sectional health survey , 2006, BMJ : British Medical Journal.

[11]  G. Brosnahan,et al.  Volume progression in polycystic kidney disease. , 2006, The New England journal of medicine.

[12]  Ping-yan Chen,et al.  Renoprotection of Optimal Antiproteinuric Doses (ROAD) Study: a randomized controlled study of benazepril and losartan in chronic renal insufficiency. , 2007, Journal of the American Society of Nephrology : JASN.

[13]  G. Remuzzi,et al.  Role of remission clinics in the longitudinal treatment of CKD. , 2008, Journal of the American Society of Nephrology : JASN.

[14]  W. Bautz,et al.  Measurement of kidney perfusion by magnetic resonance imaging: comparison of MRI with arterial spin labeling to para-aminohippuric acid plasma clearance in male subjects with metabolic syndrome. , 2010, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[15]  Hui Geng,et al.  Acute kidney injury: a springboard for progression in chronic kidney disease. , 2010, American journal of physiology. Renal physiology.

[16]  A. Yoganathan,et al.  Renal arterial blood flow measurement by breath‐held MRI: Accuracy in phantom scans and reproducibility in healthy subjects , 2010, Magnetic resonance in medicine.

[17]  Maximilian F Reiser,et al.  Diffusion and perfusion of the kidney. , 2010, European journal of radiology.

[18]  S. Francis,et al.  Multislice perfusion of the kidneys using parallel imaging: Image acquisition and analysis strategies , 2010, Magnetic resonance in medicine.

[19]  H. Hussain,et al.  Magnetization transfer helps detect intestinal fibrosis in an animal model of Crohn disease. , 2011, Radiology.

[20]  B. Brenner,et al.  Adaptation to Nephron Loss and Mechanisms of Progression in Chronic Kidney Disease , 2011 .

[21]  N. Tangri,et al.  A predictive model for progression of chronic kidney disease to kidney failure. , 2011, JAMA.

[22]  Mark Woodward,et al.  Lower estimated GFR and higher albuminuria are associated with adverse kidney outcomes. A collaborative meta-analysis of general and high-risk population cohorts. , 2011, Kidney international.

[23]  Harold I Feldman,et al.  Estimating glomerular filtration rate from serum creatinine and cystatin C. , 2012, The New England journal of medicine.

[24]  Beverley Matthews,et al.  Estimating the financial cost of chronic kidney disease to the NHS in England , 2012, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[25]  T. Lancet.  The global issue of kidney disease , 2013, The Lancet.

[26]  J. Koyner,et al.  Clinical utility of biomarkers of AKI in cardiac surgery and critical illness. , 2013, Clinical journal of the American Society of Nephrology : CJASN.

[27]  Brenda R. Hemmelgarn,et al.  Notice , 2012, Kidney International Supplements.

[28]  Bumwoo Park,et al.  Segmentation of individual renal cysts from MR images in patients with autosomal dominant polycystic kidney disease. , 2013, Clinical journal of the American Society of Nephrology : CJASN.

[29]  M. Bots,et al.  Validation of the kidney failure risk equation in European CKD patients. , 2013, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[30]  B. Jaber,et al.  AKI transition of care: a potential opportunity to detect and prevent CKD. , 2013, Clinical journal of the American Society of Nephrology : CJASN.

[31]  A. Cheung,et al.  GFR decline as an end point for clinical trials in CKD: a scientific workshop sponsored by the National Kidney Foundation and the US Food and Drug Administration. , 2014, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[32]  J. Coresh,et al.  Decline in estimated glomerular filtration rate and subsequent risk of end-stage renal disease and mortality. , 2014, JAMA.

[33]  H. Parving,et al.  Estimated GFR decline as a surrogate end point for kidney failure: a post hoc analysis from the Reduction of End Points in Non-Insulin-Dependent Diabetes With the Angiotensin II Antagonist Losartan (RENAAL) study and Irbesartan Diabetic Nephropathy Trial (IDNT). , 2014, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[34]  H. Tan,et al.  Renal perfusion imaging with two‐dimensional navigator gated arterial spin labeling , 2014, Magnetic resonance in medicine.

[35]  Erich P Huang,et al.  Metrology Standards for Quantitative Imaging Biomarkers. , 2015, Radiology.

[36]  Bradley J Erickson,et al.  Imaging classification of autosomal dominant polycystic kidney disease: a simple model for selecting patients for clinical trials. , 2015, Journal of the American Society of Nephrology : JASN.

[37]  R. Gansevoort,et al.  Albuminuria Is an Appropriate Therapeutic Target in Patients with CKD: The Pro View. , 2015, Clinical journal of the American Society of Nephrology : CJASN.

[38]  Erich P Huang,et al.  Meta-analysis of the technical performance of an imaging procedure: Guidelines and statistical methodology , 2015, Statistical methods in medical research.

[39]  Florian Kronenberg,et al.  Disease burden and risk profile in referred patients with moderate chronic kidney disease: composition of the German Chronic Kidney Disease (GCKD) cohort. , 2015, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[40]  J. Lewis,et al.  Albuminuria Is an Appropriate Therapeutic Target in Patients with CKD: The Pro View , 2015 .

[41]  G. Remuzzi,et al.  Iohexol plasma clearance for measuring glomerular filtration rate in clinical practice and research: a review. Part 2: Why to measure glomerular filtration rate with iohexol? , 2016, Clinical kidney journal.

[42]  Vicente E. Torres,et al.  The importance of total kidney volume in evaluating progression of polycystic kidney disease , 2016, Nature Reviews Nephrology.

[43]  F. Wacker,et al.  Multiparametric Functional MRI: Non-Invasive Imaging of Inflammation and Edema Formation after Kidney Transplantation in Mice , 2016, PloS one.

[44]  T. Grist,et al.  Longitudinal Assessment of Renal Perfusion and Oxygenation in Transplant Donor-Recipient Pairs Using Arterial Spin Labeling and Blood Oxygen Level-Dependent Magnetic Resonance Imaging , 2016, Investigative radiology.

[45]  C. Combe,et al.  Radiologic imaging of the renal parenchyma structure and function , 2016, Nature Reviews Nephrology.

[46]  G. Remuzzi,et al.  Iohexol plasma clearance for measuring glomerular filtration rate in clinical practice and research: a review. Part 1: How to measure glomerular filtration rate with iohexol? , 2016, Clinical kidney journal.

[47]  Frank Wacker,et al.  Diffusion‐Weighted imaging and diffusion tensor imaging detect delayed graft function and correlate with allograft fibrosis in patients early after kidney transplantation , 2016, Journal of magnetic resonance imaging : JMRI.

[48]  J. Vallée,et al.  New Magnetic Resonance Imaging Index for Renal Fibrosis Assessment: A Comparison between Diffusion-Weighted Imaging and T1 Mapping with Histological Validation , 2016, Scientific Reports.

[49]  Wim Van Biesen,et al.  Recommendations for the use of tolvaptan in autosomal dominant polycystic kidney disease: a position statement on behalf of the ERA-EDTA Working Groups on Inherited Kidney Disorders and European Renal Best Practice , 2016, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[50]  M. Burnier,et al.  Blood Oxygenation Level-Dependent MRI to Assess Renal Oxygenation in Renal Diseases: Progresses and Challenges , 2017, Front. Physiol..

[51]  C. Simmons,et al.  Could MRI Be Used To Image Kidney Fibrosis? A Review of Recent Advances and Remaining Barriers. , 2017, Clinical journal of the American Society of Nephrology : CJASN.

[52]  S. Francis,et al.  Multiparametric Renal Magnetic Resonance Imaging: Validation, Interventions, and Alterations in Chronic Kidney Disease , 2017, Front. Physiol..

[53]  D. Bolignano,et al.  Non‐proteinuric rather than proteinuric renal diseases are the leading cause of end‐stage kidney disease: Clinical Epidemiology in Nephrology , 2017, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[54]  Eyesha Hashim,et al.  Magnetic Resonance Elastography to Assess Fibrosis in Kidney Allografts. , 2017, Clinical journal of the American Society of Nephrology : CJASN.

[55]  Neil R. Powe,et al.  Global kidney health 2017 and beyond: a roadmap for closing gaps in care, research, and policy , 2017, The Lancet.

[56]  K. Kuroda,et al.  Visualization of kidney fibrosis in diabetic nephropathy by long diffusion tensor imaging MRI with spin-echo sequence , 2017, Scientific Reports.

[57]  S. Francis,et al.  Sodium MRI: a new frontier in imaging in nephrology , 2017, Current opinion in nephrology and hypertension.

[58]  J. M. Mora-Gutiérrez,et al.  Arterial spin labeling MRI is able to detect early hemodynamic changes in diabetic nephropathy , 2017, Journal of magnetic resonance imaging : JMRI.

[59]  S. Furth,et al.  Emerging biomarkers of chronic kidney disease in children , 2018, Pediatric Nephrology.

[60]  C. Laustsen,et al.  Imaging oxygen metabolism with hyperpolarized magnetic resonance: a novel approach for the examination of cardiac and renal function , 2016, Bioscience reports.

[61]  Glen R Morrell,et al.  Magnetic Resonance Imaging of the Fibrotic Kidney. , 2017, Journal of the American Society of Nephrology : JASN.

[62]  D. Buckley,et al.  Kidney volume to GFR ratio predicts functional improvement after revascularization in atheromatous renal artery stenosis , 2017, PloS one.

[63]  Laura Barisoni,et al.  Digital pathology in nephrology clinical trials, research, and pathology practice , 2017, Current opinion in nephrology and hypertension.

[64]  M. Sánchez-Niño,et al.  Clinical proteomics in kidney disease as an exponential technology: heading towards the disruptive phase , 2017, Clinical kidney journal.

[65]  Stuart A. Taylor,et al.  Imaging biomarker roadmap for cancer studies , 2016, Nature Reviews Clinical Oncology.

[66]  H. Mischak,et al.  Urinary peptide-based classifier CKD273: towards clinical application in chronic kidney disease , 2017, Clinical kidney journal.

[67]  Iosif A Mendichovszky,et al.  Renal blood oxygenation level-dependent magnetic resonance imaging to measure renal tissue oxygenation: a statement paper and systematic review , 2018, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[68]  M. Stuber,et al.  Reduced cortical oxygenation predicts a progressive decline of renal function in patients with chronic kidney disease. , 2018, Kidney international.

[69]  Ewald Moser,et al.  Magnetic resonance imaging T1- and T2-mapping to assess renal structure and function: a systematic review and statement paper , 2018, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[70]  Fabio Nery,et al.  Arterial spin labelling MRI to measure renal perfusion: a systematic review and statement paper , 2018, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[71]  George J. Dugbartey,et al.  The smell of renal protection against chronic kidney disease: Hydrogen sulfide offers a potential stinky remedy , 2018, Pharmacological reports : PR.

[72]  Nicolas Grenier,et al.  Diffusion-weighted magnetic resonance imaging to assess diffuse renal pathology: a systematic review and statement paper , 2018, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[73]  Aidan J. Delaney,et al.  Theory of signs and statistical approach to big data in assessing the relevance of clinical biomarkers of inflammation and oxidative stress , 2018, Proceedings of the National Academy of Sciences.

[74]  C. Kent.  The Effect of Social Media in Social Interaction , 2019 .